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Taxonomy and pathogenicity of Leptographium species associated with Ips subelongatus infestations of Larix spp. in northern China, including two new species

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Abstract

The larch bark beetle (Ips subelongatus), which occurs in larch plantations over a vast area of eastern Asia, infects both dying and fallen trees. When its population reaches a high density, the beetle may also infect healthy trees, resulting in tree decline and, eventually, death. Leptographium spp., in both their sexual and asexual states, are mainly associated with conifer-infesting bark beetles; some species are important tree pathogens. The aims of this study were to identify the Leptographium spp. associated with I. subelongatus infestations of Larix spp. in northern China and to examine their pathogenicity towards the tree. Morphological studies and phylogenetic approaches based on multilocus DNA sequence data (ITS2- partial r28S, partial β-tubulin, and EF-1α gene regions) showed that three Leptographium species occur in association with I. subelongatus in the areas investigated: Leptographium taigense, which is recorded in China for the first time, and two new species, namely L. innermongolicum sp. nov. and L. zhangii sp. nov. Leptographium innermongolicum is closely related to L. taigense, whereas L. zhangii belongs to the Grosmannia piceaperda species complex. The pathogenicity of these Leptographium species towards mature Larix spp. was tested by stem inoculation in forests. All inoculations only resulted in small lesions on the inner bark; therefore, the three Leptographium species were not considered to be pathogenic.

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References

  • Aoshima K (1965) Studies on wood-staining fungi of Japan. Doctoral thesis, University of Tokyo, Tokyo

  • Bakshi BK (1950) Fungi associated with ambrosia beetles in Great Britain. Trans Br Mycol Soc 33(1):111–IN11

    Article  Google Scholar 

  • De Beer ZW, Wingfield MJ (2013) Emerging lineages in the Ophiostomatales. In: Seifert KA, De Beer ZW, Wingfield MJ (eds) The ophiostomatoid fungi: expanding frontiers. CBS, Utrecht, The Netherlands, pp 21–46

    Google Scholar 

  • Eckhardt LG, Weber AM, Menard RD, Jones JP, Hess NJ (2007) Insect–fungal complex associated with loblolly pine decline in central Alabama. For Sci 53:84–92

    Google Scholar 

  • Gams W, Hoekstra ES, Aptroot A (1998) CBS course of mycology, 4th edn. Centraalbureau voor Schimmelcultures (CBS), Baarn, The Netherlands

    Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61(4):1323–1330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goidánich G (1936) II genere di Ascomiceti ‘Grosmannia’ G. Goid. Boll Staz Pat veg Roma 16:26–60

    Google Scholar 

  • Grosmann H (1931) Contributions to the knowledge concerning the life partnership between bark beetles and fungi. Z Parasitenkd 3:56–102

    Article  Google Scholar 

  • Harrington TC, Cobb FW (1988) Leptographium root diseases on conifers. American Phytopathological Society Press, St. Paul, MN

    Google Scholar 

  • Hawksworth DL (2011) A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. IMA Fungus 2:155–162. This article was first published in MycoKeys, 1:7–20 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang YT, Chen CY (2014) Leptographium globosum sp. nov., a new species with globose conidia. Mycol Progress 13:841–848

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jacobs K, Wingfield MJ (2001) Leptographium species: tree pathogens, insect associates, and agents of blue-stain. American Phytopathological Society Press, St. Paul, MN

    Google Scholar 

  • Jacobs K, Wingfield MJ (2013) An overview of Leptographium and Grosmannia. In: Seifert KA, De Beer, Wingfield MJ (eds) The ophiostomatoid fungi: expanding frontiers. CBS, Utrecht, The Netherlands, pp 47–56

  • Jacobs K, Wingfield MJ, Wingfield BD, Yamaoka Y (1998) Comparison of Ophiostoma huntii and O. europhioides and description of O. aenigmaticum sp. nov. Mycol Res 102:289–294

    Article  Google Scholar 

  • Jacobs K, Wingfield MJ, Crous PW (2000) Ophiostoma europhioides and Ceratocystis pseudoeurophioides, synonyms of O. piceaperdum. Mycol Res 104(2):238–243

    Article  Google Scholar 

  • Jacobs K, Wingfield MJ, Wingfield BD (2001) Phylogenetic relationships in Leptographium based on morphological and molecular characters. Can J Bot 79(6):719–732

    Google Scholar 

  • Jacobs K, Bergdahl DR, Wingfield MJ, Halik S, Seifert KA, Bright DE, Wingfield BD (2004) Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. Mycol Res 108(4):411–418

    Article  PubMed  Google Scholar 

  • Jacobs K, Solheim H, Wingfield BD, Wingfield MJ (2005) Taxonomic re-evaluation of Leptographium lundbergii based on DNA sequence comparisons and morphology. Mycol Res 109(10):1149–1161

    Article  CAS  PubMed  Google Scholar 

  • Jacobs K, Eckhardt LG, Wingfield MJ (2006) Leptographium profanum sp. nov., a new species from hardwood roots in North America. Can J Bot 84:759–766

    Article  Google Scholar 

  • Jacobs K, Krokene P, Solheim H, Wingfield MJ (2010) Two new species of Leptographium from Dryocetes authographus and Hylastes cunicularius in Norway. Mycol Prog 9(1):69–78

    Article  Google Scholar 

  • Katoh K, Misawa K, Kuma KI, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acid Res 30:3059–3066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kendrick WB (1962) The Leptographium complex Verticicladiella Hughes. Can J Bot 40:772–797

    Article  Google Scholar 

  • Kim JJ, Lim YW, Breuil C, Wingfield MJ, Zhou XD, Kim GH (2005) A new Leptographium species associated with Tomicus piniperda infesting pine logs in Korea. Mycol Res 109(03):275–284

    Article  CAS  PubMed  Google Scholar 

  • Kirisits T (2004) Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. In: Lieutier F, Day KR, Battisti A, Grégoire J-C, Evans HF (eds) Bark and wood boring insects in living trees in Europe, a synthesis. Kluwer, Dordrecht, The Netherlands, pp 181–235

    Chapter  Google Scholar 

  • Kirkendall LR, Faccoli M, Ye H (2008) Description of the Yunnan shoot borer, Tomicus yunnanensis Kirkendall & Faccoli sp. n. (Curculionidae, Scolytinae), an unusually aggressive pine shoot beetle from southern China, with a key to the species of Tomicus. Zootaxa 1819:25–39

    Google Scholar 

  • Lagerberg T, Lundberg G, Melin E (1927) Biological and practical researches into blueing in pine and spruce. Svenska Skogsvårdsfören Tidskr 25:145

    Google Scholar 

  • Lim YW, Alamouti SM, Kim JJ, Lee S, Breuil C (2004) Multigene phylogenies of Ophiostoma clavigerum and closely related species from bark beetle-attacked Pinus in North America. FEMS Microbiol Lett 237(1):89–96

    Article  CAS  PubMed  Google Scholar 

  • Linnakoski R, de Beer ZW, Duong TA, Niemelä P, Pappinen A, Wingfield MJ (2012) Grosmannia and Leptographium spp. associated with conifer-infesting bark beetles in Finland and Russia, including Leptographium taigense sp. nov. Antonie Van Leeuwenhoek 102:375–399

    Article  CAS  PubMed  Google Scholar 

  • Lu Q, Decock C, Zhang XY, Maraite H (2008) Leptographium sinoprocerum sp. nov., an undescribed species associated with Pinus tabuliformisDendroctonus valens in northern China. Mycologia 100:275–290

    Article  PubMed  Google Scholar 

  • Lu Q, Decock C, Zhang XY, Maraite H (2009a) Ophiostomatoid fungi (Ascomycota) associated with Pinus tabuliformis infested by Dendroctonus valens (Coleoptera) in northern China and an assessment of their pathogenicity on mature trees. Antonie Van Leeuwenhoek 96:275–293

    Article  PubMed  Google Scholar 

  • Lu M, Zhou XD, De Beer ZW, Wingfield MJ, Sun JH (2009b) Ophiostomatoid fungi associated with the invasive pine-infesting bark beetle, Dendroctonus valens, in China. Fungal Divers 38:133–145

    CAS  Google Scholar 

  • McBeath JH, Cheng M, Gay P, Ma M (2004) First report of Leptographium abietinum associated with blue stain on declining western Siberian larch in Alaska. Plant Health Progress (March):1–2

  • McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud’homme van Reine WF, Smith GF, Wiersema J, Turland NJ (eds) (2012) International Code of Nomenclature for algae, fungi, and plants (Melbourne Code). Regnum vegetabile 154. Koeltz Scientific Books, Königstein

    Google Scholar 

  • Mielke PW (1979) On asymptotic non-normality of null distributions of MRPP statistics. Commun Stat Theory Methods 8(15):1541–1550

    Article  Google Scholar 

  • Paciura D, De Beer ZW, Jacobs K, Zhou XD, Ye H, Wingfield MJ (2010) Eight new Leptographium species associated with tree-infesting bark beetles in China. Persoonia 25:94–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeffer A (1995) Zentral- und Westpaläarktische Borken- und Kernkäfer. Naturhistorishes Museum Basel, Basel, 310 pp

    Google Scholar 

  • Rayner RW (1970) A mycological colour chart. Commonwealth Mycological Institute and the British Mycological Society, Kew, Surrey

  • Sallé A, Monclus R, Yart A, Garcia J, Romary P, Lieutier F (2005) Fungal flora associated with Ips typographus: frequency, virulence, and ability to stimulate the host defence reaction in relation to insect population levels. Can J For Res 35:365–373

    Article  Google Scholar 

  • Seifert KA, Webber JF, Wingfield MJ (1993) Methods for studying species of Ophiostoma and Ceratocystis. In: Wingfield MJ, Seifert KA, Webber JF (eds) Ceratocystis and Ophiostoma: taxonomy, ecology and pathogenicity. American Phytopathological Society Press, St. Paul, MN, pp 255–259

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stauffer C, Kirisits T, Nussbaumer C, Pavlin R, Wingfield MJ (2001) Phylogenetic relationships between the European and Asian eight spined larch bark beetle populations (Coleoptera, Scolytidae) inferred from DNA sequences and fungal associates. Eur J Entomol 98:99–105

    Article  CAS  Google Scholar 

  • Swofford DL (2001) PAUP*: Phylogenetic analysis using parsimony (and other methods) 4.0.b5

  • Swofford DL (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA

  • Van der Westhuizen K, Wingfield MJ, Yamaoka Y, Kemp GHJ, Crous PW (1995) A new species of Ophiostoma with a Leptographium anamorph from larch in Japan. Mycol Res 99(11):1334–1338

    Article  Google Scholar 

  • Wagener WW, Mielke JL (1961) A staining-fungus root disease of pondersoa, Jeffrey, and pinyon pines. Plant Dis Rep 45:831–835

    Google Scholar 

  • White TJ, Bruns T, Lee SJWT, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc Guide Methods Appl 18(1):315–322

    Google Scholar 

  • Wingfield MJ, Capretti P, Mackenzie M (1988) Leptographium spp. as root pathogens on conifers. An international perspective. In: Harrington TC, Cobb FW Jr (eds) Leptographium root diseases on conifers. American Phytopathological Society Press, St. Paul, MN, pp 113–128

    Google Scholar 

  • Wingfield MJ, Seifert KA, Webber JF (1993) Ceratocystis and Ophiostoma: taxonomy, ecology and pathogenicity. American Phytopathological Society Press, St. Paul, MN

    Google Scholar 

  • Wood SL, Bright DE (1992) A catalog of Scolytidae and Platypodidae (Coleoptera), Part 2: Taxonomic Index Volume A. Great Basin Naturalist Memoirs, No. 13. Brigham Young University, Provo, UT, 833 pp

    Google Scholar 

  • Yamaoka Y, Wingfield MJ, Takahashi I, Solheim H (1997) Ophiostomatoid fungi associated with the spruce bark beetle Ips typographus f. japonicus in Japan. Mycol Res 101:1215–1227

    Article  Google Scholar 

  • Yamaoka Y, Wingfield MJ, Ohsawa M, Kuroda Y (1998) Ophiostomatoid fungi associated with Ips cembrae in Japan and their pathogenicity of Japanese larch. Mycoscience 39:367–378

    Article  Google Scholar 

  • Yamaoka Y, Masuya H, Chung WH, Goto H, To-Anun C, Tokumasu S, Zhou X, Wingfield MJ (2008) The teleomorph of Leptographium yunnanense, discovered in crosses among isolates from Thailand, China, and Japan. Mycoscience 49:233–240

    Article  Google Scholar 

  • Yamaoka Y, Chung WH, Masuya H, Hizai M (2009) Constant association of ophiostomatoid fungi with the bark beetle Ips subelongatus invading Japanese larch logs. Mycoscience 50:165–172

    Article  Google Scholar 

  • Yang JL, Lin Q, Chen GF (2007) Risk analysis of Ips subelongatus Motschulsky. J Northeast For Univ 35(3):60–63

    CAS  Google Scholar 

  • Yin HF, Huang FS, Li ZL (1984) Economic insect fauna of China. Science and Technology Press, Beijing, pp 54–55

    Google Scholar 

  • Yin M, Duong TA, Wingfield MJ, Zhou X, De Beer ZW (2015) Taxonomy and phylogeny of the Leptographium procerum complex, including Leptographium sinense sp. nov. and Leptographium longiconidiophorum sp. nov. Antonie Van Leeuwenhoek 107:547–563

    Article  PubMed  Google Scholar 

  • Zhou XD, Jacobs K, Morelet M, Ye H, Lieutier F, Wingfield MJ (2000) A new Leptographium species associated with Tomicus piniperda in southwestern China. Mycoscience 41:573–578

    Article  Google Scholar 

  • Zhou XD, De Beer ZW, Harrington TC, McNew D, Kirisits T, Wingfield MJ (2004) Epitypification of Ophiostoma galeiformis and phylogeny of species in the O. galeiformis complex. Mycologia 96:1306–1315

    Article  PubMed  Google Scholar 

  • Zhou XD, Jacobs K, Kirisits T, Chhetri DB, Wingfield MJ (2008) Leptographium bhutanense sp. nov., associated with the root collar weevil Hylobitelus chenkupdorjii on Pinus wallichiana in Bhutan. Persoonia Molecular Phylogeny Evol Fungi 21(1):1–8

    Article  Google Scholar 

  • Zipfel RD, De Beer ZW, Jacobs K, Wingfield BD, Wingfield MJ (2006) Multi-gene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Stud Mycol 55:75–97

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was supported by the Special Fund for Forest Scientific Research in the Public Welfare (201204501), the National Natural Science Foundation of China (project no.: 31070571), and the Special Fund for Public Welfare Institutes of the Central Government (CAFRIFEEP201102). This work was conducted under the auspices of the Chinese Academy of Forestry International Cooperation and Innovation Team. Quan Lu gratefully acknowledges a postdoctoral scholarship granted by the Wallonia-Brussels International Excellent Grants Program. Cony Decock gratefully acknowledges the financial support received from the Belgian State and Belgian Federal Science Policy through the BCCM™ research program.

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Liu, XW., Wang, HM., Lu, Q. et al. Taxonomy and pathogenicity of Leptographium species associated with Ips subelongatus infestations of Larix spp. in northern China, including two new species. Mycol Progress 16, 1–13 (2017). https://doi.org/10.1007/s11557-016-1245-1

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